Swarming of <i>Pseudomonas aeruginosa</i> Is Dependent on Cell-to-Cell Signaling and Requires Flagella and Pili

Journal of Bacteriology - Tập 182 Số 21 - Trang 5990-5996 - 2000
Thilo Köhler1, Lasta Kocjancic Curty1, Francisco Barja2, Christian van Delden1, Jean-Claude Péchère1
1Department of Genetics and Microbiology, University Medical Center,1 and
2Laboratory of General Microbiology, Sciences III, University of Geneva,2 CH-1211 Geneva 4, Switzerland

Tóm tắt

ABSTRACT We describe swarming in Pseudomonas aeruginosa as a third mode of surface translocation in addition to the previously described swimming and twitching motilities. Swarming in P. aeruginosa is induced on semisolid surfaces (0.5 to 0.7% agar) under conditions of nitrogen limitation and in response to certain amino acids. Glutamate, aspartate, histidine, or proline, when provided as the sole source of nitrogen, induced swarming, while arginine, asparagine, and glutamine, among other amino acids, did not sustain swarming. Cells from the edge of the swarm were about twice as long as cells from the swarm center. In both instances, bacteria possessing two polar flagella were observed by light and electron microscopy. While a fliC mutant of P. aeruginosa displayed slightly diminished swarming, a pilR and a pilA mutant, both deficient in type IV pili, were unable to swarm. Furthermore, cells with mutations in the las cell-to-cell signaling system showed diminished swarming behavior, while rhl mutants were completely unable to swarm. Evidence is presented for rhamnolipids being the actual surfactant involved in swarming motility, which explains the involvement of the cell-to-cell signaling circuitry of P. aeruginosa in this type of surface motility.

Từ khóa


Tài liệu tham khảo

Allison C. Lai H. C. Gygi D. Hughes C. Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells.Mol. Microbiol.819935360

Arino S. Marchal R. Vandecasteele J. P. Involvement of a rhamnolipid-producing strain of Pseudomonas aeruginosa in the degradation of polycyclic aromatic hydrocarbons by a bacterial community.J. Appl. Microbiol.841998769776

10.1128/jb.150.2.956-959.1982

10.1128/jb.178.3.831-839.1996

10.1139/m80-022

10.1128/jb.177.24.7155-7163.1995

Burkart M. Toguchi A. Harshey R. M. The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli.Proc. Natl. Acad. Sci. USA95199825682573

10.1128/IAI.67.7.3207-3214.1999

10.1126/science.284.5418.1318

10.1128/jb.164.2.544-549.1985

10.1128/jb.154.2.780-786.1983

Darzins A. Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus.Mol. Microbiol.111994137153

10.1128/JB.182.2.357-364.2000

Eberl L. Winson M. K. Sternberg C. Stewart G. S. Christiansen G. Chhabra S. R. Bycroft B. Williams P. Molin S. Givskov M. Involvement of N-acyl-l-hormoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens.Mol. Microbiol.201996127136

10.1128/JB.181.5.1623-1629.1999

10.1128/jb.155.3.1446-1449.1983

10.1128/iai.62.10.4572-4579.1994

10.1111/j.1365-2958.1995.mmi_17061167.x

10.1016/S0378-1119(97)00116-9

Harshey R. M. Bees aren't the only ones: swarming in gram-negative bacteria.Mol. Microbiol.131994389394

Harshey R. M. Matsuyama T. Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells.Proc. Natl. Acad. Sci. USA91199486318635

Hobbs M. Collie E. S. Free P. D. Livingston S. P. Mattick J. S. PilS and PilR, a two-component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa.Mol. Microbiol.71993669682

Ishimoto K. S. Lory S. Formation of pilin in Pseudomonas aeruginosa requires the alternative sigma factor (RpoN) of RNA polymerase.Proc. Natl. Acad. Sci. USA86198919541957

10.1128/jb.174.11.3514-3521.1992

Kato J. Nakamura T. Kuroda A. Ohtake H. Cloning and characterization of chemotaxis genes in Pseudomonas aeruginosa.Biosci. Biotechnol. Biochem.631999155161

Latifi A. Foglino M. Tanaka K. Williams P. Lazdunski A. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS.Mol. Microbiol.21199611371146

Latifi A. Winson M. K. Foglino M. Bycroft B. W. Stewart G. S. Lazdunski A. Williams P. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1.Mol. Microbiol.171995333343

10.1128/JB.180.23.6384-6388.1998

Liu P. V. Extracellular toxins of Pseudomonas aeruginosa.J. Infect. Dis.130 (Suppl.)1974S94S99

Maniatis T. Fritsch E. F. Sambrook J. Molecular cloning: a laboratory manual. 1982 Cold Spring Harbor Laboratory Cold Spring Harbor N.Y

10.1128/jb.177.4.948-952.1995

Morales V. M. Bäckman A. Bagdasarian M. A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants.Gene9719913947

10.1128/jb.139.1.137-140.1979

Ochsner U. A. Fiechter A. Reiser J. Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis.J. Biol. Chem.26919941978719795

10.1128/jb.176.7.2044-2054.1994

Ochsner U. A. Reiser J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa.Proc. Natl. Acad. Sci. USA92199564246428

10.1128/JB.182.2.425-431.2000

O'Toole G. A. Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development.Mol. Microbiol.301998295304

10.1126/science.8493556

Pearson J. P. Gray K. M. Passador L. Tucker K. D. Eberhard A. Iglewski B. H. Greenberg E. P. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes.Proc. Natl. Acad. Sci. USA911994197201

Pearson J. P. Passador L. Iglewski B. H. Greenberg E. P. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa.Proc. Natl. Acad. Sci. USA92199514901494

10.1128/jb.179.18.5756-5767.1997

10.1128/jb.179.10.3127-3132.1997

Rashid M. H. Kornberg A. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa.Proc. Natl. Acad. Sci. USA97200048854890

Saiman L. Ishimoto K. Lory S. Prince A. The effect of piliation and exoproduct expression on the adherence of Pseudomonas aeruginosa to respiratory epithelial monolayers.J. Infect. Dis.1611990541548

Siegmund I. Wagner F. New method for detecting rhamnolipids excreted by Pseudomonas species during growth in mineral agar.Biotechnol. Tech.51991265268

Spangenberg C. Fislage R. Sierralta W. Tummler B. Romling U. Comparison of type IV-pilin genes of Pseudomonas aeruginosa of various habitats has uncovered a novel unusual sequence.FEMS Microbiol. Lett.1251995265273

Spangenberg C. Heuer T. Burger C. Tummler B. Genetic diversity of flagellins of Pseudomonas aeruginosa.FEBS Lett.3961996213217

Taguchi K. Fukutomi H. Kuroda A. Kato J. Ohtake H. Genetic identification of chemotactic transducers for amino acids in Pseudomonas aeruginosa.Microbiology143199732233229

10.1128/iai.63.4.1278-1285.1995

10.1128/iai.64.1.37-43.1996

10.3201/eid0404.980405

10.1016/0378-1119(91)90221-V